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Distribution and Function of Carbonic Anhydrase Related Proteins (Carps) VIII, X and XI

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Distribution and Function of Carbonic Anhydrase Related Proteins (Carps) VIII, X and XI ASHOK ASPATWAR Distribution and Function of Carbonic Anhydrase Related Proteins (CARPs) VIII, X and XI ACADEMIC DISSERTATION To be presented, with the permission of the Board of the BioMediTech of the University of Tampere, for public discussion in the Main Auditorium of Building B, School of Medicine of the University of Tampere, Medisiinarinkatu 3, Tampere, on October 31st, 2014, at 12 o’clock. UNIVERSITY OF TAMPERE ASHOK ASPATWAR Distribution and Function of Carbonic Anhydrase Related Proteins (CARPs) VIII, X and XI Acta Universitatis Tamperensis 1981 Tampere University Press Tampere 2014 ACADEMIC DISSERTATION University of Tampere, BioMediTech Finland Supervised by Reviewed by Professor Mauno Vihinen Professor Matti Airaksinen University of Lund University of Helsinki Sweden Finland Professor Seppo Parkkila Professor Todd Alexander University of Tampere University of Alberta Finland Canada The originality of this thesis has been checked using the Turnitin OriginalityCheck service in accordance with the quality management system of the University of Tampere. Copyright ©2014 Tampere University Press and the author Cover design by Mikko Reinikka Distributor: [email protected] http://granum.uta.fi Acta Universitatis Tamperensis 1981 Acta Electronica Universitatis Tamperensis 1468 ISBN 978-951-44-9594-6 (print) ISBN 978-951-44-9595-3 (pdf) ISSN-L 1455-1616 ISSN 1456-954X ISSN 1455-1616 http://tampub.uta.fi Suomen Yliopistopaino Oy – Juvenes Print Tampere 2014 441 729 Painotuote Contents Contents ....................................................................................................................................... 3 List of original communications .............................................................................................. 6 Abbreviations .............................................................................................................................. 7 Abstract ........................................................................................................................................ 9 1 Introduction ..................................................................................................................... 11 2 Review of the literature .................................................................................................. 12 2.1 Carbonic anhydrases .............................................................................................. 12 2.1.1 Historical aspects of carbonic anhydrase isozymes...................................... 12 2.2 Carbonic anhydrase related proteins ................................................................... 12 2.3 General properties of CARP VIII ....................................................................... 15 2.3.1 Expression of CARP VIII in animal models ................................................ 15 2.3.2 Expression of CARP VIII in humans and human cell line ........................ 16 2.3.3 Crystal structure of CARP VIII and its interaction with ITPR1 ............... 17 2.3.4 Role of Car8 gene in gait disorder in mouse ................................................. 19 2.3.5 Association of CA8 gene with ataxia in humans .......................................... 19 2.3.6 Role of CARP VIII in cancer and other diseases ......................................... 21 2.3.7 Catalytic activity and inhibition of mutant CARP VIII ............................... 23 2.4 General properties of CARP X ........................................................................... 24 2.4.1 Expression of CARP X in human and mouse tissues ................................. 24 2.4.2 Expression of CARP X in pathological conditions ..................................... 25 2.4.3 Catalytic activity and inhibition of mutant CARP X ................................... 26 2.5 General properties of CARP XI .......................................................................... 26 2.5.1 Expression of CARP XI in normal tissues .................................................... 27 2.5.2 Expression of CARP XI in pathological conditions .................................... 28 2.5.3 Catalytic activity and inhibition of mutant CARP XI .................................. 29 3 3 Aims and objectives of the study .................................................................................. 30 4 Materials and methods ................................................................................................... 31 4.1 Bioinformatic analysis of CARP VIII, X and XI sequences (I) ..................... 31 4.2 Expression of CARP genes (I, III, and IV) ...................................................... 31 4.2.1 Extraction of mRNA from mouse and zebrafish ........................................ 31 4.2.2 Synthesis of single strand cDNA and RT-qPCR.......................................... 32 4.2.3 Immunohistochemistry of CARPs in mouse and zebrafish (I, III).......... 33 4.2.4 Bioinformatic analysis of CARP VIII (III) ................................................... 34 4.2.5 Bioinformatic analysis of CARP X and XI sequences (IV) ........................ 34 4.3 Molecular analysis of CARPs in zebrafish (III, IV) ......................................... 35 4.3.1 Zebrafish husbandry for the knockdown experiments (III, IV) ............... 35 4.3.2 Sequencing of zebrafish CARP genes (III, IV) ........................................... 36 4.3.3 Knockdown of CARP genes using morpholinos (III, IV) ........................ 36 4.3.4 Analysis of CARP VIII protein and CARP mRNAs (III, IV) .................. 36 4.3.5 Live image analysis of zebrafish phenotypes (III, IV) ................................ 37 4.3.6 Histochemical analysis of morphant and control larvae (III, IV) ............. 37 4.3.7 Assay to detect apoptotic cell death in morphant fish (III, IV) ................ 38 4.3.8 Electron microscope analysis (III) ................................................................. 38 4.3.9 Cloning of human CA10 and CA11 genes in pcDNA3.1 .......................... 39 4.3.10 Synthesis of mRNA and rescue of ca10a and ca10b morphants ................. 39 5 Results ............................................................................................................................... 40 5.1 Distribution and expression of CARP VIII, X and XI sequences................. 40 5.1.1 Distribution and evolutionary analysis of CARP sequences (I) ................. 40 5.1.2 Expression analysis of CARPs in mouse tissues (I) ..................................... 41 5.1.3 Comparative analysis of CARP VIII sequence (II, III) ............................. 42 5.1.4 Bioinformatic analysis of zebrafish CARPs and their genes (III, IV) ...... 43 5.1.5 Features of secretory proteins in CARPX-like sequences .......................... 43 5.1.6 Expression analysis of CARP genes in zebrafish (III, IV) ......................... 44 5.1.7 ca8 knockdown leads to developmental defects in zebrafish (III) ............ 45 5.1.8 Suppression of ca10a and ca10b genes leads to phenotypic defects (IV) .. 46 5.1.9 Morphological changes and apoptosis in morphant fish (III, IV). ........... 47 5.1.10 Abnormal swim pattern in ca8, ca10a and ca10b morphants (III, IV) ...... 47 6 Discussion ........................................................................................................................ 48 4 6.1 Bioinformatic and molecular analysis of CARP sequences ............................. 48 6.1.1 The CARPs are widely distributed across species (I, IV) ........................... 48 6.1.2 CARPs are mainly expressed in the CNS (I) ................................................ 50 6.1.3 Sequence and structural analysis of CARP VIII (II) ................................... 51 6.1.4 Zebrafish CARP VIII and ITPR1 sequences are coevolved (III)............. 52 6.1.5 The ca8 morphants displayed abnormal swim pattern (III) ....................... 52 6.1.6 Zebrafish ca10a and ca10b genes are widely expressed (IV) ....................... 54 6.1.7 Ataxia and apoptosis in ca10a and ca10b morphants (IV) ........................... 56 7 Summary and future directions ..................................................................................... 57 Acknowledgements .................................................................................................................. 59 References.................................................................................................................................. 64 Original communications ........................................................................................................ 70 5 List of original communications This thesis is based on the following original communications, which are referred to in the text by their Roman numerals (I-IV) I. Aspatwar A, Tolvanen ME, Parkkila S. 2010. Phylogeny and expression of carbonic anhydrase-related proteins. BMC Mol Biol. 11:25. II. Aspatwar A, Tolvanen M, Ortutay C, Parkkila S. 2010. Carbonic anhydrase related protein VIII and its role in neurodegeneration and cancer. Curr Pharm Des. 16:3264-76. III. Aspatwar A, Tolvanen MEE, Jokitalo E, Parikka M, Ortutay C, Rämet M, Vihinen M, Parkkila S. 2013. Abnormal cerebellar development and ataxia in CARP VIII morphant zebrafish. Hum Mol Genet. 22:417-32. IV. Aspatwar A, Tolvanen MEE, Barker H, Ortutay C, Pan P, Kuuslahti M, Parikka M, Rämet M, Parkkila S. 2014. Abnormal embryonic development and movement pattern in ca10a and ca10b morphant zebrafish. Submitted. The original publications have been reproduced
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